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Seasonal antibacterial activity of two red seaweeds, Palmaria palmata and Grateloupia turuturu, on European abalone pathogen Vibrio harveyi

Published online by Cambridge University Press:  16 December 2014

Nuria García-Bueno ,
Priscilla Decottignies ,
Vincent Turpin ,
Justine Dumay ,
Christine Paillard ,
Valérie Stiger-Pouvreau ,
Nelly Kervarec ,
Yves-François Pouchus ,
Arnaldo Aitor Marín-Atucha  and
Joël Fleurence
Nuria García-Bueno
Affiliation:
Université de Nantes, Institut Universitaire Mer et Littoral, EA 2160 Mer Molécules Santé, 2 rue de la Houssinière, BP 92208, 44322 Nantes Cedex 3, France Departamento de Ecología e Hidrología, Facultad de Biología, Universidad de Murcia, 30100 Murcia, Spain
Priscilla Decottignies
Affiliation:
Université de Nantes, Institut Universitaire Mer et Littoral, EA 2160 Mer Molécules Santé, 2 rue de la Houssinière, BP 92208, 44322 Nantes Cedex 3, France
Vincent Turpin
Affiliation:
Université de Nantes, Institut Universitaire Mer et Littoral, EA 2160 Mer Molécules Santé, 2 rue de la Houssinière, BP 92208, 44322 Nantes Cedex 3, France
Justine Dumay
Affiliation:
Université de Nantes, Institut Universitaire Mer et Littoral, EA 2160 Mer Molécules Santé, 2 rue de la Houssinière, BP 92208, 44322 Nantes Cedex 3, France
Christine Paillard
Affiliation:
Laboratoire des sciences de l’environnement marin (LEMAR), Institut universitaire européen de la mer (IUEM), place Copernic Technopôle Brest-Iroise, 29280 Plouzané, France
Valérie Stiger-Pouvreau
Affiliation:
Laboratoire des sciences de l’environnement marin (LEMAR), Institut universitaire européen de la mer (IUEM), place Copernic Technopôle Brest-Iroise, 29280 Plouzané, France
Nelly Kervarec
Affiliation:
Service RMN-RPE, UFR Sciences et Techniques, avenue Le Gorgeu, 29200 Brest Cedex, France
Yves-François Pouchus
Affiliation:
Université de Nantes, Institut Universitaire Mer et Littoral, EA 2160 Mer Molécules Santé, 2 rue de la Houssinière, BP 92208, 44322 Nantes Cedex 3, France
Arnaldo Aitor Marín-Atucha
Affiliation:
Departamento de Ecología e Hidrología, Facultad de Biología, Universidad de Murcia, 30100 Murcia, Spain
Joël Fleurence*
Affiliation:
Université de Nantes, Institut Universitaire Mer et Littoral, EA 2160 Mer Molécules Santé, 2 rue de la Houssinière, BP 92208, 44322 Nantes Cedex 3, France
*
a Corresponding author: joel.fleurence@univ-nantes.fr
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Abstract

Vibrio harveyi is the main pathogen of the European abalone Haliotis tuberculata, and recently caused important mortalities at the production sites of this marine gastropod in France. In the present work, the monthly antibacterial activity of two red seaweed species from the French Atlantic coast, the native Palmaria palmata and the introduced Grateloupia turuturu, were investigated against the abalone pathogen Vibrio harveyi strain ORM4. Water-soluble extracts were screened using the microplate method. Grateloupia turuturu showed an antibacterial activity with a maximal growth inhibition in spring of around 16%. In contrast, Palmaria palmata was inactive, as further growth of the bacteria was observed. Preliminary one-dimensional proton nuclear magnetic-resonance (1H NMR) profiles identified the differences between the two water-soluble extracts.

Keywords

Antibacterial activityGrowth inhibitionImmunityWater-soluble extractsVibrio harveyiHaliotis tuberculata
Type
Research Article
Information
Aquatic Living Resources , Volume 27 , Issue 2 , April 2014 , pp. 83 - 89
Copyright
© EDP Sciences, IFREMER, IRD 2014

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References

Austin, B., Zhang, X., 2006, Vibrio harveyi: a significant pathogen of marine vertebrates and invertebrates. Lett. Appl. Microbiol. 43, 119–124. CrossRefGoogle ScholarPubMed
Bansemir, A., Blume, M., Schröder, S., Lindequist, U., 2006, Screening of cultivated seaweeds for antibacterial activity against fish pathogenic bacteria. Aquaculture 252, 79–84. CrossRefGoogle Scholar
Bazes, A., Silkina, A., Defer, D., Bernède-Bauduin, C., Quéméner, E., Braud, J.-P., Bourgougnon, N., 2006, Active substances from Ceramium botryocarpum used as antifouling products in aquaculture. Aquaculture 258, 664–674. CrossRefGoogle Scholar
Bhakuni D.S., Rawat D.S., 2005, Bioactive marine natural products. Springer, NY.
Bondad-Reantaso, M.G., Subasinghe, R.P., Arthur, J.R., Ogawa, K., Chinabut, S., Adlard, R., Tan, Z., Shariff, M., 2005, Disease and health management in Asian aquaculture. Vet. Parasitol. 132, 249–272. CrossRefGoogle ScholarPubMed
Bourgaud, F., Gravot, A., Milesi, S., Gontier, E., 2001, Production of plant secondary metabolites: a historical perspective. Plant Sci. 161, 839–851. CrossRefGoogle Scholar
Bradford, M.M., 1976, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254. CrossRefGoogle ScholarPubMed
Caccamese, S., Azzolina, R., Furnari, G., Cormaci, M., Grasso, S., 1980, Antimicrobial and antiviral activities of extracts from mediterranean algae. Bot. Mar. 23, 285–288. Google Scholar
Cardozo, K.H., Guaratini, T., Barros, M.P., Falcão, V.R., Tonon, A.P., Lopes, N.P., Pinto, E., 2007, Metabolites from algae with economical impact. Comp. Biochem. Physiol. Part C: Toxicol. Pharmacol. 146, 60–78. Google ScholarPubMed
Chaplin M.F., Kennedy J.F., 1994, Carbohydrate analysis: a practical approach. IRL Press.
Cox, S., Abu-Ghannam, N., Gupta, S., 2010, An assessment of the antioxidant and antimicrobial activity of six species of edible Irish seaweeds. Int. Food Res. J. 17, 205–220. Google Scholar
Cronin, G., Hay, M.E., 1996, Susceptibility to herbivores depends on recent history of both the plant and animal. Ecology 77, 1531–1543. CrossRefGoogle Scholar
Cronin, G., Paul, V.J., Hay, M.E., Fenical, W., 1997, Are tropical herbivores more resistant than temperate herbivores to seaweed chemical defenses? Diterpenoid metobolites from Dictyota acutiloba as feeding deterrents for tropical versus temperate fishes and urchins. J. Chem. Ecol. 23, 289–302. CrossRefGoogle Scholar
Demetropoulos, C., Langdon, C., 2004, Pacific dulse (Palmaria mollis) as a food and biofilter in recirculated, land-based abalone culture systems. Aquac. Eng. 32, 57–75. CrossRefGoogle Scholar
Denis, C., Morançais, M., Gaudin, P., Fleurence, J., 2009, Effect of enzymatic digestion on thallus degradation and extraction of hydrosoluble compounds from Grateloupia turuturu. Bot. Mar. 52, 262–267. CrossRefGoogle Scholar
Eguía, E., Trueba, A., 2007, Application of marine biotechnology in the production of natural biocides for testing on environmentally innocuous antifouling coatings. J. Coatings Techn. Res. 4, 191–202. CrossRefGoogle Scholar
FAO, 2013, Statistiques des pêches et de l’aquaculture, modules de requêtes en ligne. FAO Comput. Inf. Ser. Fish.
Freile-Pelegrin, Y., Morales, J.L., 2004, Antibacterial activity in marine algae from the coast of Yucatan, Mexico. Bot. Mar. 47, 140–146. CrossRefGoogle Scholar
Galland-Irmouli, A.-V., Fleurence, J., Lamghari, R., Luçon, M., Rouxel, C., Barbaroux, O., Bronowicki, J.-P., Villaume, C., Guéant, J.-L., 1999, Nutritional value of proteins from edible seaweed Palmaria palmata (dulse). J. Nutr. Biochem. 10, 353–359. CrossRefGoogle Scholar
Garnier, M., Labreuche, Y., Garcia, C., Robert, M., Nicolas, J.-L., 2007, Evidence for the involvement of pathogenic bacteria in summer mortalities of the Pacific oyster Crassostrea gigas. Microb. Ecol. 53, 187–196. CrossRefGoogle ScholarPubMed
Gay, M., Renault, T., Pons, A.-M., Le Roux, F., 2004, Two Vibrio splendidus related strains collaborate to kill Crassostrea gigas: taxonomy and host alterations. Dis. Aquat. Org. 62, 65–74. CrossRefGoogle ScholarPubMed
Genovese, G., Faggio, C., Gugliandolo, C., Torre, A., Spano, A., Morabito, M., Maugeri, T.L., 2012, In vitro evaluation of antibacterial activity of Asparagopsis taxiformis from the Straits of Messina against pathogens relevant in aquaculture. Mar. Biol. Res. 73, 1–6. Google ScholarPubMed
Goecke, F., Labes, A., Wiese, J., Imhoff, J.F., 2010, Chemical interactions between marine macroalgae and bacteria. Mar. Ecol. Prog. Ser. 409, 267–300. CrossRefGoogle Scholar
Gupta, S., Abu-Ghannam, N., 2011, Bioactive potential and possible health effects of edible brown seaweeds. Trends Food Sci. Tech. 22, 315–326. CrossRefGoogle Scholar
Hellio, C., Bremer, G., Pons, A., Le Gal, Y., Bourgougnon, N., 2000, Inhibition of the development of microorganisms (bacteria and fungi) by extracts of marine algae from Brittany, France. Appl. Microbiol. Biotechnol. 54, 543–549. CrossRefGoogle ScholarPubMed
Hellio, C., De La Broise, D., Dufossé, L., Le Gal, Y., Bourgougnon, N., 2001, Inhibition of marine bacteria by extracts of macroalgae: potential use for environmentally friendly antifouling paints. Mar. Environ. Res. 52, 231–247. CrossRefGoogle ScholarPubMed
Holmström, K., Gräslund, S., Wahlström, A., Poungshompoo, S., Bengtsson, B.E., Kautsky, N., 2003, Antibiotic use in shrimp farming and implications for environmental impacts and human health. Int. J. Food. Sci. Technol. 38, 255–266. CrossRefGoogle Scholar
Hornsey, I., Hide, D., 1974, The production of antimicrobial compounds by British marine algae I. Antibiotic-producing marine algae. Br. Phycol. J. 9, 353–361. CrossRefGoogle Scholar
Hornsey, I., Hide, D., 1976, The production of antimicrobial compounds by British marine algae II. Seasonal variation in production of antibiotics. Br. Phycol. J. 11, 63–67. Google Scholar
Huchette, S., Clavier, J., 2004, Status of the ormer (Haliotis tuberculata L.) industry in Europe. J. Shellfish Res. 23, 951–956. Google Scholar
Hudson, J.B., Kim, J.H., Lee, M.K., DeWreede, R.E., Hong, Y.K., 1998, Antiviral compounds in extracts of Korean seaweeds: Evidence for multiple activities. J. Appl. Phycol. 10, 427–434. CrossRefGoogle Scholar
Jiang, H.-F., Liu, X.-L., Chang, Y.-Q., Liu, M.-T., Wang, G.-X., 2013, Effects of dietary supplementation of probiotic Shewanella colwelliana WA64, Shewanella olleyana WA65 on the innate immunity and disease resistance of abalone, Haliotis discus hannai Ino. Fish Shellfish Immunol. 35, 86–91. CrossRefGoogle ScholarPubMed
Kesarcodi-Watson, A., Kaspar, H., Lategan, M.J., Gibson, L., 2008, Probiotics in aquaculture: the need, principles and mechanisms of action and screening processes. Aquaculture 274, 1–14. CrossRefGoogle Scholar
Kumar, K.A., Rengasamy, R., 2000, Antibacterial activities of seaweed extracts/fractions obtained through a TLC profile against the phytopathogenic bacterium Xanthomonas oryzae pv. oryzae. Bot. Mar. 43, 417–421. Google Scholar
Lacoste, A., Jalabert, F., Malham, S., Cueff, A., Gelebart, F., Cordevant, C., Lange, M., Poulet, S., 2001, A Vibrio splendidus strain is associated with summer mortality of juvenile oysters Crassostrea gigas in the Bay of Morlaix (North Brittany, France). Dis. Aquat. Org. 46, 139–145. CrossRefGoogle Scholar
LeGall, L., Deniaud, E., Rusig, A.-M., 2004, Etude de la phenologie de la reproduction de la Rhodophyceae Palmaria palmata le long des cotes francaises de la Manche. Cah. Biol. Mar. 45, 269–275. Google Scholar
Mabeau, S., Fleurence, J., 1993, Seaweed in food products: biochemical and nutritional aspects. Trends Food Sci. Technol. 4, 103–107. CrossRefGoogle Scholar
Mai, K., Mercer, J.P., Donlon, J., 1995, Comparative studies on the nutrition of two species of abalone, Haliotis tuberculata L. and Haliotis discus hannai Ino. IV. Optimum dietary protein level for growth. Aquaculture 136, 165–180. Google Scholar
Martí, R., Uriz, M.J., Ballesteros, E., Turon, X., 2004, Benthic assemblages in two Mediterranean caves: species diversity and coverage as a function of abiotic parameters and geographic distance. J. Mar. Biol. Assoc. 84, 557–572. CrossRefGoogle Scholar
Mata, L., Wright, E., Owens, L., Paul, N., De Nys, R., 2013, Water-soluble natural products from seaweed have limited potential in controlling bacterial pathogens in fish aquaculture J. Appl. Phycol. 25(6), 1963–1973. CrossRefGoogle Scholar
Morgan, K., Simpson, F., 1981, Cultivation of Palmaria palmata (Rhodymenia): Effect of high concentrations of nitrate and ammonium on growth and nitrogen uptake. Aquat. Bot. 11, 167–171. CrossRefGoogle Scholar
Morgan, K., Wright, L., Simpson, F., 1980, Review of chemical constituents of the red alga Palmaria palmata (dulse). Econ. Bot. 34, 27–50. CrossRefGoogle Scholar
Munier M., Dumay J., Morançais M., Jaouen P., Fleurence J., 2013, Variation in the biochemical composition of the edible seaweed Grateloupia turuturu Yamada harvested from two sampling sites on the Brittany coast (France): The influence of storage method on the extraction of the seaweed pigment R-phycoerythrin. J. Chem. 2013, 8.
Nicolas, J.-L., Basuyaux, O., Mazurie, J., Thebault, A., 2002, Vibrio carchariae, a pathogen of the abalone Haliotis tuberculata. Dis. Aquat. Org. 50, 35–43. CrossRefGoogle ScholarPubMed
Paillard, C., 2004a, A short-review of brown ring disease, a vibriosis affecting clams, Ruditapes philippinarum and Ruditapes decussatus. Aquat. Living. Resour. 17, 467–475. CrossRefGoogle Scholar
Paillard, C., Le Roux, F., Borrego, J.J., 2004b, Bacterial disease in marine bivalves, a review of recent studies: trends and evolution. Aquat. Living. Resour. 17, 477–498. CrossRefGoogle Scholar
Paillard, C., Korsnes, K., Le Chevalier, P., Le Boulay, C., Harkestad, L.S., Eriksen, A.G., Willassen, E., Bergh, Ø., Bovo, C., Skår, C.K., 2008, Vibrio tapetis-like strain isolated from introduced Manila clams Ruditapes philippinarum showing symptoms of brown ring disease in Norway. Dis. Aquat. Org. 81, 153–161. CrossRefGoogle ScholarPubMed
Pang, S., Xiao, T., Shan, T., Wang, Z., Gao, S., 2006, Evidences of the intertidal red alga Grateloupia turuturu in turning Vibrio parahaemolyticus into non-culturable state in the presence of light. Aquaculture 260, 369–374. CrossRefGoogle Scholar
Plouguerné E., 2006, Etude écologique et chimique de deux algues introduites sur les côtes bretonnes, Grateloupia turuturu Yamada et Sargassum muticum (Yendo) Fensholt : nouvelles ressources biologiques de composés à activité antifouling. Thèse dr chimie marine, Université de Bretagne Occidentale, Brest.
Plouguerné, E., Kikuchi, H., Oshima, Y., Deslandes, E., Stiger-Pouvreau, V., 2006, Isolation of cholest-5-en-3-ol formate from the red alga Grateloupia turuturu Yamada and its chemotaxonomic significance. Biochem. Syst. Ecol. 34, 714–717. CrossRefGoogle Scholar
Plouguerné, E., Hellio, C., Deslandes, E., Veron, B., Stiger-Pouvreau, V., 2008, Anti-microfouling activities in extracts of two invasive algae: Grateloupia turuturu and Sargassum muticum. Bot. Mar. 51, 202–208. CrossRefGoogle Scholar
Prado, S., Romalde, J.L., Barja, J.L., 2010, Review of probiotics for use in bivalve hatcheries. Vet. Microbiol. 145, 187–197. CrossRefGoogle ScholarPubMed
Rosen, G., Langdon, C.J., Evans, F., 2000, The nutritional value of Palmaria mollis cultured under different light intensities and water exchange rates for juvenile red abalone Haliotis rufescens. Aquaculture 185, 121–136. CrossRefGoogle Scholar
Simon-Colin, C., Kervarec, N., Pichon, R., Bessières, M.-A., Deslandes, E., 2002, Characterization of N-methyl-L-methionine sulfoxide and isethionic acid from the red alga Grateloupia doryphora. Phycol. Res. 50, 125–128. CrossRefGoogle Scholar
Simon, C., Gall, E.A., Deslandes, E., 2001, Expansion of the red alga Grateloupia doryphora along the coasts of Brittany (France). Hydrobiologia 443, 23–29. CrossRefGoogle Scholar
Travers, M.-A., Basuyaux, O., Le Goïc, N., Huchette, S., Nicolas, J.-L., Koken, M., Paillard, C., 2009, Influence of temperature and spawning effort on Haliotis tuberculata mortalities caused by Vibrio harveyi: an example of emerging vibriosis linked to global warming. Global Change Biol. 15, 1365–1376. CrossRefGoogle Scholar
Val, A., Platas, G., Basilio, A., Cabello, A., Gorrochategui, J., Suay, I., Vicente, F., Portillo, E., Río, M., Reina, G., 2001, Screening of antimicrobial activities in red, green and brown macroalgae from Gran Canaria (Canary Islands, Spain). Int. Microbiol. 4, 35–40. Google Scholar
Vlachos, V., Critchley, A., von Holy, A., 1998, Antimicrobial activity of extracts from selected southern African marine macroalgae. South Afr. J. Sci. 93, 328–332. Google Scholar
Wang, T., Jónsdóttir, R., Kristinsson, H.G., Hreggvidsson, G.O., Jónsson, J.O., Thorkelsson, G., Ólafsdóttir, G., 2010, Enzyme-enhanced extraction of antioxidant ingredients from red algae Palmaria palmata. Food Sci. Technol. 43, 1387–1393. Google Scholar
Wang, Y.-B., Li, J.-R., Lin, J., 2008, Probiotics in aquaculture: challenges and outlook. Aquaculture 281, 1–4. CrossRefGoogle Scholar
Wu, C.-J., Wang, H., Chan, Y.-L., Li, T.-L., 2011, Passive immune-protection of small abalone against Vibrio alginolyticus infection by anti-Vibrio IgY-encapsulated feed. Fish Shellfish Immunol. 30, 1042–1048. CrossRefGoogle ScholarPubMed
Yates J., Peckol P., 1993, Effects of nutrient availability and herbivory on polyphenolics in the seaweed Fucus vesiculosus. Ecology 1757–1766.
Zhang, X.H., Austin, B., 2000, Pathogenicity of Vibrio harveyi to salmonids. J. Fish Dis. 23, 93–102. CrossRefGoogle Scholar